Cell-specific type I IFN signatures in autoimmunity and viral infection: what makes the difference?
Gene expression profiling of peripheral blood mononuclear cells (PBMCs) has revealed a crucial role for type I interferon (IFN) in the pathogenesis of systemic lupus erythematosus (SLE). However, it is unclear how particular leucocyte subsets contribute to the overall type I IFN signature of PBMCs a...
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| Veröffentlicht in: | PloS one 2013-12, Vol.8 (12), p.e83776-e83776 |
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| creator | Kyogoku, Chieko Smiljanovic, Biljana Grün, Joachim R Biesen, Robert Schulte-Wrede, Ursula Häupl, Thomas Hiepe, Falk Alexander, Tobias Radbruch, Andreas Grützkau, Andreas |
| description | Gene expression profiling of peripheral blood mononuclear cells (PBMCs) has revealed a crucial role for type I interferon (IFN) in the pathogenesis of systemic lupus erythematosus (SLE). However, it is unclear how particular leucocyte subsets contribute to the overall type I IFN signature of PBMCs and whole blood samples.Furthermore, a detailed analysis describing the differences in the IFN signature in autoimmune diseases from that observed after viral infection has not been performed to date. Therefore, in this study, the transcriptional responses in peripheral T helper cells (CD4(+)) and monocyte subsets (CD16(-) inflammatory and CD16(+) resident monocytes) isolated from patients with SLE, healthy donors (ND) immunised with the yellow fever vaccine YFV-17Dand untreated controls were compared by global gene expression profiling.It was striking that all of the transcripts that were regulated in response to viral exposure were also found to be differentially regulated in SLE, albeit with markedly lower fold-change values. In addition to this common IFN signature, a pathogenic IFN-associated gene signature was detected in the CD4(+) T cells and monocytes from the lupus patients. IL-10, IL-9 and IL-15-mediated JAK/STAT signalling was shown to be involved in the pathological amplification of IFN responses observed in SLE. Type I IFN signatures identified were successfully applied for the monitoring of interferon responses in PBMCs of an independent cohort of SLE patients and virus-infected individuals. Moreover, these cell-type specific gene signatures allowed a correct classification of PBMCs independent from their heterogenic cellular composition. In conclusion, our data show for the first time that monocytes and CD4 cells are sensitive biosensors to monitor type I interferon response signatures in autoimmunity and viral infection and how these transriptional responses are modulated in a cell- and disease-specific manner. |
| doi_str_mv | 10.1371/journal.pone.0083776 |
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However, it is unclear how particular leucocyte subsets contribute to the overall type I IFN signature of PBMCs and whole blood samples.Furthermore, a detailed analysis describing the differences in the IFN signature in autoimmune diseases from that observed after viral infection has not been performed to date. Therefore, in this study, the transcriptional responses in peripheral T helper cells (CD4(+)) and monocyte subsets (CD16(-) inflammatory and CD16(+) resident monocytes) isolated from patients with SLE, healthy donors (ND) immunised with the yellow fever vaccine YFV-17Dand untreated controls were compared by global gene expression profiling.It was striking that all of the transcripts that were regulated in response to viral exposure were also found to be differentially regulated in SLE, albeit with markedly lower fold-change values. In addition to this common IFN signature, a pathogenic IFN-associated gene signature was detected in the CD4(+) T cells and monocytes from the lupus patients. IL-10, IL-9 and IL-15-mediated JAK/STAT signalling was shown to be involved in the pathological amplification of IFN responses observed in SLE. Type I IFN signatures identified were successfully applied for the monitoring of interferon responses in PBMCs of an independent cohort of SLE patients and virus-infected individuals. Moreover, these cell-type specific gene signatures allowed a correct classification of PBMCs independent from their heterogenic cellular composition. In conclusion, our data show for the first time that monocytes and CD4 cells are sensitive biosensors to monitor type I interferon response signatures in autoimmunity and viral infection and how these transriptional responses are modulated in a cell- and disease-specific manner.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0083776</identifier><identifier>PMID: 24391825</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adult ; Analysis ; Autoimmune diseases ; Autoimmunity ; B cells ; Bacterial infections ; Biological response modifiers ; Biology ; Biomarkers - metabolism ; Biosensors ; Blood ; Case-Control Studies ; CD16 antigen ; CD4 antigen ; CD4-Positive T-Lymphocytes - immunology ; CD4-Positive T-Lymphocytes - metabolism ; Chronic conditions ; Cytokines ; Disease ; Fc receptors ; Female ; Fever ; Gene expression ; Gene Expression Profiling ; Genes ; Genomics ; Health aspects ; Healthy Volunteers ; Helper cells ; Humans ; Immunization ; Immunology ; Infection ; Infections ; Inflammation ; Interferon ; Interferon Type I - genetics ; Interleukin 10 ; Interleukin 15 ; Interleukin 9 ; Leukocytes (mononuclear) ; Leukocytes, Mononuclear - immunology ; Leukocytes, Mononuclear - metabolism ; Lupus ; Lupus Erythematosus, Systemic - blood ; Lupus Erythematosus, Systemic - genetics ; Lupus Erythematosus, Systemic - immunology ; Lymphocytes ; Lymphocytes T ; Medical research ; Medicine ; Monocytes ; Monocytes - immunology ; Monocytes - metabolism ; Oligonucleotide Array Sequence Analysis ; Pathogenesis ; Pathogens ; Patients ; Peripheral blood mononuclear cells ; Real-Time Polymerase Chain Reaction ; Reverse Transcriptase Polymerase Chain Reaction ; Rheumatism ; Rheumatoid arthritis ; Rheumatology ; RNA, Messenger - genetics ; Signal Transduction ; Signaling ; Signatures ; Studies ; Systemic lupus erythematosus ; T cells ; Transcription ; Vector-borne diseases ; Viral infections ; Viruses ; Yellow fever ; Yellow Fever - genetics ; Yellow Fever - immunology ; Yellow Fever - prevention & control ; Yellow Fever Vaccine - administration & dosage ; Yellow fever virus - genetics</subject><ispartof>PloS one, 2013-12, Vol.8 (12), p.e83776-e83776</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Kyogoku et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2013 Kyogoku et al 2013 Kyogoku et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c758t-54d7dca4e82a8246fc894f9a3c268b44746a5e5f41f1abc96c335fa9d49f19fe3</citedby><cites>FETCH-LOGICAL-c758t-54d7dca4e82a8246fc894f9a3c268b44746a5e5f41f1abc96c335fa9d49f19fe3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3877094/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3877094/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24391825$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Bobé, Pierre</contributor><creatorcontrib>Kyogoku, Chieko</creatorcontrib><creatorcontrib>Smiljanovic, Biljana</creatorcontrib><creatorcontrib>Grün, Joachim R</creatorcontrib><creatorcontrib>Biesen, Robert</creatorcontrib><creatorcontrib>Schulte-Wrede, Ursula</creatorcontrib><creatorcontrib>Häupl, Thomas</creatorcontrib><creatorcontrib>Hiepe, Falk</creatorcontrib><creatorcontrib>Alexander, Tobias</creatorcontrib><creatorcontrib>Radbruch, Andreas</creatorcontrib><creatorcontrib>Grützkau, Andreas</creatorcontrib><title>Cell-specific type I IFN signatures in autoimmunity and viral infection: what makes the difference?</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Gene expression profiling of peripheral blood mononuclear cells (PBMCs) has revealed a crucial role for type I interferon (IFN) in the pathogenesis of systemic lupus erythematosus (SLE). However, it is unclear how particular leucocyte subsets contribute to the overall type I IFN signature of PBMCs and whole blood samples.Furthermore, a detailed analysis describing the differences in the IFN signature in autoimmune diseases from that observed after viral infection has not been performed to date. Therefore, in this study, the transcriptional responses in peripheral T helper cells (CD4(+)) and monocyte subsets (CD16(-) inflammatory and CD16(+) resident monocytes) isolated from patients with SLE, healthy donors (ND) immunised with the yellow fever vaccine YFV-17Dand untreated controls were compared by global gene expression profiling.It was striking that all of the transcripts that were regulated in response to viral exposure were also found to be differentially regulated in SLE, albeit with markedly lower fold-change values. In addition to this common IFN signature, a pathogenic IFN-associated gene signature was detected in the CD4(+) T cells and monocytes from the lupus patients. IL-10, IL-9 and IL-15-mediated JAK/STAT signalling was shown to be involved in the pathological amplification of IFN responses observed in SLE. Type I IFN signatures identified were successfully applied for the monitoring of interferon responses in PBMCs of an independent cohort of SLE patients and virus-infected individuals. Moreover, these cell-type specific gene signatures allowed a correct classification of PBMCs independent from their heterogenic cellular composition. In conclusion, our data show for the first time that monocytes and CD4 cells are sensitive biosensors to monitor type I interferon response signatures in autoimmunity and viral infection and how these transriptional responses are modulated in a cell- and disease-specific manner.</description><subject>Adult</subject><subject>Analysis</subject><subject>Autoimmune diseases</subject><subject>Autoimmunity</subject><subject>B cells</subject><subject>Bacterial infections</subject><subject>Biological response modifiers</subject><subject>Biology</subject><subject>Biomarkers - metabolism</subject><subject>Biosensors</subject><subject>Blood</subject><subject>Case-Control Studies</subject><subject>CD16 antigen</subject><subject>CD4 antigen</subject><subject>CD4-Positive T-Lymphocytes - immunology</subject><subject>CD4-Positive T-Lymphocytes - metabolism</subject><subject>Chronic conditions</subject><subject>Cytokines</subject><subject>Disease</subject><subject>Fc receptors</subject><subject>Female</subject><subject>Fever</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>Genes</subject><subject>Genomics</subject><subject>Health aspects</subject><subject>Healthy Volunteers</subject><subject>Helper cells</subject><subject>Humans</subject><subject>Immunization</subject><subject>Immunology</subject><subject>Infection</subject><subject>Infections</subject><subject>Inflammation</subject><subject>Interferon</subject><subject>Interferon Type I - genetics</subject><subject>Interleukin 10</subject><subject>Interleukin 15</subject><subject>Interleukin 9</subject><subject>Leukocytes (mononuclear)</subject><subject>Leukocytes, Mononuclear - immunology</subject><subject>Leukocytes, Mononuclear - metabolism</subject><subject>Lupus</subject><subject>Lupus Erythematosus, Systemic - blood</subject><subject>Lupus Erythematosus, Systemic - genetics</subject><subject>Lupus Erythematosus, Systemic - immunology</subject><subject>Lymphocytes</subject><subject>Lymphocytes T</subject><subject>Medical research</subject><subject>Medicine</subject><subject>Monocytes</subject><subject>Monocytes - immunology</subject><subject>Monocytes - metabolism</subject><subject>Oligonucleotide Array Sequence Analysis</subject><subject>Pathogenesis</subject><subject>Pathogens</subject><subject>Patients</subject><subject>Peripheral blood mononuclear cells</subject><subject>Real-Time Polymerase Chain Reaction</subject><subject>Reverse Transcriptase Polymerase Chain Reaction</subject><subject>Rheumatism</subject><subject>Rheumatoid arthritis</subject><subject>Rheumatology</subject><subject>RNA, Messenger - genetics</subject><subject>Signal Transduction</subject><subject>Signaling</subject><subject>Signatures</subject><subject>Studies</subject><subject>Systemic lupus erythematosus</subject><subject>T cells</subject><subject>Transcription</subject><subject>Vector-borne diseases</subject><subject>Viral infections</subject><subject>Viruses</subject><subject>Yellow fever</subject><subject>Yellow Fever - genetics</subject><subject>Yellow Fever - immunology</subject><subject>Yellow Fever - prevention & control</subject><subject>Yellow Fever Vaccine - administration & dosage</subject><subject>Yellow fever virus - genetics</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk1tv0zAUxyMEYmPwDRBEQkLw0OJb4ngPoKliUGliErdXy7GPW48kLrEz6LfHpdnUoD0gP9jy-Z2_fW5Z9hSjOaYcv7nyQ9-pZr7xHcwRqijn5b3sGAtKZiVB9P7B-Sh7FMIVQgWtyvJhdkQYFbgixXGmF9A0s7AB7azTedxuIF_my_NPeXCrTsWhh5C7LldD9K5th87Fba46k1-7XjXJYkFH57vT_NdaxbxVPxIf15AbZy300Gl49zh7YFUT4Mm4n2Tfzt9_XXycXVx-WC7OLmaaF1WcFcxwoxWDiqiKsNLqSjArFNWkrGrGOCtVAYVl2GJVa1FqSgurhGHCYmGBnmTP97qbxgc55idIzDilDKOCJGK5J4xXV3LTu1b1W-mVk38vfL-Sqo9ONyCpJSVDxJiaAKsMrmtbCVRYEAaAG5S03o6vDXULRkMXU0YmolNL59Zy5a8lrThHgiWBV6NA738OEKJsXdCpHKoDP-z-LVApKkpEQl_8g94d3UitVAoglcand_VOVJ4xzgXhhOJEze-g0jLQOp2aybp0P3F4PXFITITfcaWGEOTyy-f_Zy-_T9mXB-waVBPXwTfDrp3CFGR7UPc-hB7sbZIxkrtZuMmG3M2CHGchuT07LNCt003z0z8KMQSi</recordid><startdate>20131231</startdate><enddate>20131231</enddate><creator>Kyogoku, Chieko</creator><creator>Smiljanovic, Biljana</creator><creator>Grün, Joachim R</creator><creator>Biesen, Robert</creator><creator>Schulte-Wrede, Ursula</creator><creator>Häupl, Thomas</creator><creator>Hiepe, Falk</creator><creator>Alexander, Tobias</creator><creator>Radbruch, Andreas</creator><creator>Grützkau, Andreas</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20131231</creationdate><title>Cell-specific type I IFN signatures in autoimmunity and viral infection: what makes the difference?</title><author>Kyogoku, Chieko ; Smiljanovic, Biljana ; Grün, Joachim R ; Biesen, Robert ; Schulte-Wrede, Ursula ; Häupl, Thomas ; Hiepe, Falk ; Alexander, Tobias ; Radbruch, Andreas ; Grützkau, Andreas</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c758t-54d7dca4e82a8246fc894f9a3c268b44746a5e5f41f1abc96c335fa9d49f19fe3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Adult</topic><topic>Analysis</topic><topic>Autoimmune diseases</topic><topic>Autoimmunity</topic><topic>B cells</topic><topic>Bacterial infections</topic><topic>Biological response modifiers</topic><topic>Biology</topic><topic>Biomarkers - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kyogoku, Chieko</au><au>Smiljanovic, Biljana</au><au>Grün, Joachim R</au><au>Biesen, Robert</au><au>Schulte-Wrede, Ursula</au><au>Häupl, Thomas</au><au>Hiepe, Falk</au><au>Alexander, Tobias</au><au>Radbruch, Andreas</au><au>Grützkau, Andreas</au><au>Bobé, Pierre</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cell-specific type I IFN signatures in autoimmunity and viral infection: what makes the difference?</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2013-12-31</date><risdate>2013</risdate><volume>8</volume><issue>12</issue><spage>e83776</spage><epage>e83776</epage><pages>e83776-e83776</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Gene expression profiling of peripheral blood mononuclear cells (PBMCs) has revealed a crucial role for type I interferon (IFN) in the pathogenesis of systemic lupus erythematosus (SLE). However, it is unclear how particular leucocyte subsets contribute to the overall type I IFN signature of PBMCs and whole blood samples.Furthermore, a detailed analysis describing the differences in the IFN signature in autoimmune diseases from that observed after viral infection has not been performed to date. Therefore, in this study, the transcriptional responses in peripheral T helper cells (CD4(+)) and monocyte subsets (CD16(-) inflammatory and CD16(+) resident monocytes) isolated from patients with SLE, healthy donors (ND) immunised with the yellow fever vaccine YFV-17Dand untreated controls were compared by global gene expression profiling.It was striking that all of the transcripts that were regulated in response to viral exposure were also found to be differentially regulated in SLE, albeit with markedly lower fold-change values. In addition to this common IFN signature, a pathogenic IFN-associated gene signature was detected in the CD4(+) T cells and monocytes from the lupus patients. IL-10, IL-9 and IL-15-mediated JAK/STAT signalling was shown to be involved in the pathological amplification of IFN responses observed in SLE. Type I IFN signatures identified were successfully applied for the monitoring of interferon responses in PBMCs of an independent cohort of SLE patients and virus-infected individuals. Moreover, these cell-type specific gene signatures allowed a correct classification of PBMCs independent from their heterogenic cellular composition. In conclusion, our data show for the first time that monocytes and CD4 cells are sensitive biosensors to monitor type I interferon response signatures in autoimmunity and viral infection and how these transriptional responses are modulated in a cell- and disease-specific manner.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24391825</pmid><doi>10.1371/journal.pone.0083776</doi><tpages>e83776</tpages><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2013-12, Vol.8 (12), p.e83776-e83776 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1473341052 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Adult Analysis Autoimmune diseases Autoimmunity B cells Bacterial infections Biological response modifiers Biology Biomarkers - metabolism Biosensors Blood Case-Control Studies CD16 antigen CD4 antigen CD4-Positive T-Lymphocytes - immunology CD4-Positive T-Lymphocytes - metabolism Chronic conditions Cytokines Disease Fc receptors Female Fever Gene expression Gene Expression Profiling Genes Genomics Health aspects Healthy Volunteers Helper cells Humans Immunization Immunology Infection Infections Inflammation Interferon Interferon Type I - genetics Interleukin 10 Interleukin 15 Interleukin 9 Leukocytes (mononuclear) Leukocytes, Mononuclear - immunology Leukocytes, Mononuclear - metabolism Lupus Lupus Erythematosus, Systemic - blood Lupus Erythematosus, Systemic - genetics Lupus Erythematosus, Systemic - immunology Lymphocytes Lymphocytes T Medical research Medicine Monocytes Monocytes - immunology Monocytes - metabolism Oligonucleotide Array Sequence Analysis Pathogenesis Pathogens Patients Peripheral blood mononuclear cells Real-Time Polymerase Chain Reaction Reverse Transcriptase Polymerase Chain Reaction Rheumatism Rheumatoid arthritis Rheumatology RNA, Messenger - genetics Signal Transduction Signaling Signatures Studies Systemic lupus erythematosus T cells Transcription Vector-borne diseases Viral infections Viruses Yellow fever Yellow Fever - genetics Yellow Fever - immunology Yellow Fever - prevention & control Yellow Fever Vaccine - administration & dosage Yellow fever virus - genetics |
| title | Cell-specific type I IFN signatures in autoimmunity and viral infection: what makes the difference? |
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